The role of food in the spread of the Methicillin – resistant Staphylococcus aureus (MRSA) Methicillin – resistance Staphylococcus aureus in food
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Abstract
Methicillin-resistant Staphylococcus aureus (MRSA) are important human pathogen. It is present in a wide range of animal species (pigs, cows, sheep, and chickens) even in healthy animals. Identification of MRSA in foods has led to concerns about the role of livestock in the epidemiology of MRSA infections in human. This review focuses on the spread of MRSA in different types of food and its antimicrobial resistance to the most widely used antimicrobials in human and veterinary medicine. The results of review indicates that livestock is major source of MRSA in humans and mainly transmitted to humans through contaminated food. The actual prevalence of MRSA in animals and food as well as impact to the human health is not well understood. It is clearly that MRSA is an important pathogen to veterinary medicine and human health which requires more and in-depth research to understand the hazard and take effective measures to limit it.
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References
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Archer GL. Staphylococcus aureus: a well-armed pathogen. Clinical Infection Disease, 1998, 26(5): 1179-1181. https://doi.org/10.1086/520289
Bangieva D, Rusev V. Risk from Staphylococcus aureus in informally marketed raw cow milk. Food Science and Applied Biotechnology, 2019, 2(1): 74-80. https://doi.org/10.30721/fsab2019.v2.i1.67
Barber M. Methicillin-resistance staphylococci. Journal of Clinical Pathology, 1961, 14(4): 385-393. http://doi.org/10.1136/jcp.14.4.385
Bywater R., Deluyker H., Deroover E., de Jong A., Marion H., McConville M., Rowan T., Shryock T., Shuster D., Thomas V., Valle T., Walters J. A European survey of antimicrobial susceptibility among zoonotic and commensal bacteria isolated from food-producing animals. Journal of Antimicrobial Chemotherapy, 2004, 54(4): 744-745. https://doi.org/10.1093/jac/dkh422
De Neeling A.J., van den Broek M.J., Spalburg E.C., van Sauten-Verheuvel M.G., Dam-Deisz W.D., Boshuizen H.C., van de Giessen A.W., van Dijkeren F., Huijsdens X.W. High prevalence of methicillin-resistance Staphylococcus aureus in pigs. Veterinary Microbiology, 2007, 122(3-4): 366-372. http://doi.org/10.1016/j.vetmic.2007.01.027
Devriese L.A., Hommez J. Epidemiology of methicillin-resistance Staphylococcus aureus in dairy herds. Research in Veterinary Science, 1975, 19(1): 23-27. https://doi.org/10.1016/S0034-5288(18)33549-5
El-Razika K.A., Arafab A.A., Ibrahim E.S., El-Shater N.S., El-Demerdash G.O., El-Shinawye M.N., Elmahallawy E.K. Phenotypic and genotypic characterization of tetracycline resistant Staphylococcus aureus isolated from food of animal origin. Egyptian Journal of Environmental Research, 2017, 9(10): 63-90.
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Farahmand S., Haeili M., Darban-Sarokhalil D. Molecular typing and drug resistance patterns of Staphylococcus aureus isolated from raw beef and chicken meat samples. Iranian Journal of Medical Microbiology, 2020, 14(5): 478-489. https://doi.org/10.30699/ijmm.14.5.468
Gogov, Y. Investigation on methicillin-resistant strains Staphylococuus aureus (MRSA) isolated from animal origin foodstuffs. Veterinarna sbirka, 2011, 3-4: 30-33 [in Bulgarian]
Goudarzi M., Seyedjavadi S.S., Nasiri M.J., Goudorzi H., Sajadi Nia R., Dabiri H. Molecular characteristics of methicillin-resistance Staphylococcus aureus (MRSA) strains isolated from patient with bacteremia based on MLST, SCCmec, spa and agr locus types analysis. Microbial Pathogenesis, 2017, 104(3): 328-335. http://doi.org/10.1016/j.micpath.2017.01.055
Hennekinne J., DeBuyser M., Dragacci S. Staphylococcus aureus and its food poisoning toxins: characterization and outbreak investigation. FEMS Microbiology Reviews, 2012, 36(4): 815-836. http://doi.org/10.1111/j.1574-6976.2011.00311.x
Ivanova T., Gurova-Mehmedova E., Daskalov H. Case study of staphylococcal enterotoxin poisoning after consumption of ready-to-eat roasted chicken products. Bulgarian Journal of Agricultural Science, 2017, 23(1): 159-164. Available at: https://www.agrojournal.org/23/01-23.pdf
Jackson C.R., Davis J.A., Barrett J.B. Prevalence and characterization of methicillin-resistant Staphylococcus aureus isolates from retail meat and humans in Georgia. Journal of Clinical Microbiology, 2013, 51(4): 1199–1207. http://doi.org/10.1128/JCM.03166-12.
Kalupahana R.S., Duim B., Verstappen K.M., Gamage C.D., Dissanayake N., Ranatunga L., Graveland H., Wagenaar J.A. MRSA in pigs and the environment as a risk for employees in pig-dense areas of Sri Lanka. Frontiers in Sustainable Food Systems, 2019, 3(2019): 25. http://doi.org/10.3389/fsufs.2019.00025
Kim Y., Kim H., Kim S., Kim M., Kwak H. Prevalence and characteristics of antimicrobial-resistant Staphylococcus aureus and methicillin-resistance Staphylococcus aureus from retail meat in Korea. Food Science of Animal Resources, 2020, 40(5): 758-771. https://doi.org/10.5851/kosfa.2020.e50
Lakhundi S., Zhang K. Methicillin-resistant Staphylococcus aureus: molecular characterization, evolution and epidemiology. Clinical Microbiology Reviews, 2018, 31(4): e00020-18. https://doi.org/10.1128/CMR.00020-18
Lowy F.D. Medical progress: Staphylococcus aureus infections. New England Journal of Medicine, 1998, 339(8): 520-532. https://doi.org/10.1056/NEJM199808203390806
Mahros M., Mohamed S., Khalid A.E., Sallam I. Multidrug-, methicillin-, and vancomycin-resistant Staphylococcus aureus isolated from ready-to-eat meat sandwiches: An ongoing food and public health concern. International Journal of Food Microbiology, 2021, 346(5): 109165. https://doi.org/10.1016/j.ijfoodmicro.2021.109165
Neyra R.C., Frisancho J.A., Rinsky J.L., Resnick C., Carroll K.C., Rule A.M., Ross T., You Y., Price L.B., Silbergeld E.K. Multidrug-resistant and methicillin-resistant Staphylococcus aureus (MRSA) in hog slaughter and processing plant workers and their community in North Carolina (USA). Environmental Health Perspectives, 2014, 122(5): 471-477. http://www.doi.org/10.1289/ehp.1306741
O’Brien A., Hanson B., Farina S., Wu J., Simmering J., Wardyn S., Forshey B., Kulick M., Wallinga D., Smith T. MRSA in conventional and alternative retail pork products. PLoS ONE, 2012, 7(1): e30092. https://doi.org/10.1371/journal.pone.0030092
Özdemir H., Keyvan E. Isolation and characterisation of Staphylococcus aureus strains isolated from beef, sheep and chicken meat. Ankara Üniversitesi Veteriner Fakültesi Dergisi, 2016, 63(4): 333-338. https://doi.org/10.1501/Vetfak_0000002749
Pu S., Han F., Ge B. Isolation and characterization of methicillin-resistant Staphylococcus aureus from Louisiana retail meats. Applied and Environmental Microbiology, 2009, 75(1): 265-267. http://doi.org/10.1128/AEM.01110-08
Sadi A., Samad M., Saddam, Basharat N., Ali S., Roohullah, Saad Z., Khan A.N., Ahmad Y., Khan A. and Khan J. Methicillin-resistant Staphylococcus aureus (MRSA) in slaughter houses and meat shops in capital territory of Pakistan during 2018–2019. Frontiers in Microbiology, 2020, 11(9): 577707. http://doi.org/10.3389/fmicb.2020.577707
Studenica A., Märtlbauer E., Mulliqi-Osmani G. The prevalenceof bacterial contaminants in artisanal cheese sold in informal markets. The case of Kosovo. Food Science and Applied Biotechnology, 2022, 5(1): 77-86. https://doi.org/10.30721/fsab2022.v5.i1.168
Tacconelli E. Methicillin-resistant Staphylococcus aureus: Source control and surveillance organisation. Clin Microbiol Infect, 2009, 15: 31-38. https://doi.org/10.1111/j.14690691.2009.03096.x
Tang Y., Larsen J., Kjeldgaard J., Andersena S.P., Skov R., Ingmera H. Methicillin-resistant and –susceptible Staphylococcus aureus from retail meat in Denmark. International Journal of Food Microbiology, 2017, 246(5): 72-76. https://doi.org/10.1016/j.ijfoodmicro.2017.03.001
Tanomsridachchai W., Changkaew K., Changkwanyeun R., Prapasawat W., Intarapuk A., Fukushima Y., Yamasamit N., Flav Kapalamula T., Nakajima C., Suthienkul O., Suzuki Y. Antimicrobial resistance and molecular characterization of methicillin-resistant Staphylococcus aureus isolated from slaughtered pigs and pork in the Central region of Thailand. Antibiotics, 2021, 10(2): 206. https://doi.org/10.3390/antibiotics10020206
Tiemersa E.W., Bronzwaer SLAM, Lyytikainen O., Degener J.E., Schrijnemakers P., Bruinsma N., Monen J., Witte W., Grundmann H. European antimicrobial resistance surveillance system participants. Methicillin-resistance Staphyloccus aureus in Europe, 1999-2002. Emerging Infectious Diseases, 2004, 10(9): 1627-1634. http://doi.org/10.3201/eid1009.040069
van Duijkeren E., Ikawaty R., Broekhuizen Stins M.J., Jansen M.D., Spalburg E.C., deNeeling A.J., Allaart J.C., van Nes A., Wagenaar J.A., Fluit A.C. Transmission of methicillin-resistant Staphylococcus aureus strains between different kinds of pig farms. Veterinary Microbiology, 2008, 126(4): 383-389. https://doi.org/10.1016/j.vetmic.2007.07.021
van Loo H.M., Diederen M.W., Savelkoul P., Woudenberg J., Roosendaal R., van Belkum A., Lemmens-den Toom N., Verhulst C., van Keulen P., Kluytmans J. Methicillin-Resistant Staphylococcus aureus in meat products, the Netherlands. Emerging Infectious Diseases, 2007, 13(11): 1753-1755. http://doi.org/10.3201/eid1311.070358 Weese J.S., Avery B.P., Reid-Smith R.J. Detection and quantification of methicillin-resistant Staphylococcus aureus (MRSA) clones in retail meat products. Letters in Applied Microbiology, 2010, 51(3): 338-342. https://doi.org/10.1111/j.1472-765X.2010.02901.x
Wells M., Juett B. Prevalence of MRSA on meat products in central Kentucky. Bios, 2012, 83(1): 33-38. https://www.jstor.org/stable/23267857
Wu S., Huang J., Wu Q., Zhang J., Zhang F., Yang X., Wu H., Zeng H., Chen M., Ding Y et al. Staphylococcus aureus isolated from retail meat and meat products in China: Incidence, antibiotic resistance and genetic diversity. Frontiers in Microbiology, 2018, 9(11): 02767. http://doi.org/10.3389/fmicb.2018.02767
Wu S., Huang J., Zhang F., Wu Q., Zhang J., Pang R., Zeng H., Yang X., Chen M., Wang J., Dai J., Xue L., Lei T., Wei X. Prevalence and characterization of food-related methicillin-resistance Staphylococcus aureus (MRSA) in China. Frontiers in Microbiology, 2019, 10(2): 00304. https://doi.org/10.3389/fmicb.2019.00304
Wu S, Zhang F, Huang J, Wu Q, Zhang J, Dai J, Zeng H, Yang X, Chen M, Pang R et al. Phenotypic and genotypic characterization of PVL-positive Staphylococcus aureus isolated from retail foods in China. International Journal of Food Microbiology, 2018, 304(9): 119-126. http://doi.org/10.1016/j.ijfoodmicro.2019.05.021
Archer GL. Staphylococcus aureus: a well-armed pathogen. Clinical Infection Disease, 1998, 26(5): 1179-1181. https://doi.org/10.1086/520289
Bangieva D, Rusev V. Risk from Staphylococcus aureus in informally marketed raw cow milk. Food Science and Applied Biotechnology, 2019, 2(1): 74-80. https://doi.org/10.30721/fsab2019.v2.i1.67
Barber M. Methicillin-resistance staphylococci. Journal of Clinical Pathology, 1961, 14(4): 385-393. http://doi.org/10.1136/jcp.14.4.385
Bywater R., Deluyker H., Deroover E., de Jong A., Marion H., McConville M., Rowan T., Shryock T., Shuster D., Thomas V., Valle T., Walters J. A European survey of antimicrobial susceptibility among zoonotic and commensal bacteria isolated from food-producing animals. Journal of Antimicrobial Chemotherapy, 2004, 54(4): 744-745. https://doi.org/10.1093/jac/dkh422
De Neeling A.J., van den Broek M.J., Spalburg E.C., van Sauten-Verheuvel M.G., Dam-Deisz W.D., Boshuizen H.C., van de Giessen A.W., van Dijkeren F., Huijsdens X.W. High prevalence of methicillin-resistance Staphylococcus aureus in pigs. Veterinary Microbiology, 2007, 122(3-4): 366-372. http://doi.org/10.1016/j.vetmic.2007.01.027
Devriese L.A., Hommez J. Epidemiology of methicillin-resistance Staphylococcus aureus in dairy herds. Research in Veterinary Science, 1975, 19(1): 23-27. https://doi.org/10.1016/S0034-5288(18)33549-5
El-Razika K.A., Arafab A.A., Ibrahim E.S., El-Shater N.S., El-Demerdash G.O., El-Shinawye M.N., Elmahallawy E.K. Phenotypic and genotypic characterization of tetracycline resistant Staphylococcus aureus isolated from food of animal origin. Egyptian Journal of Environmental Research, 2017, 9(10): 63-90.
European Food Safety Authority (EFSA) and European Centre for Disease prevention and Control (ECDC). The European Union summary report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2017/20108. EFSA J., 2020, 18(3): 607. Available at: http://www.efsa.europa.eu
Farahmand S., Haeili M., Darban-Sarokhalil D. Molecular typing and drug resistance patterns of Staphylococcus aureus isolated from raw beef and chicken meat samples. Iranian Journal of Medical Microbiology, 2020, 14(5): 478-489. https://doi.org/10.30699/ijmm.14.5.468
Gogov, Y. Investigation on methicillin-resistant strains Staphylococuus aureus (MRSA) isolated from animal origin foodstuffs. Veterinarna sbirka, 2011, 3-4: 30-33 [in Bulgarian]
Goudarzi M., Seyedjavadi S.S., Nasiri M.J., Goudorzi H., Sajadi Nia R., Dabiri H. Molecular characteristics of methicillin-resistance Staphylococcus aureus (MRSA) strains isolated from patient with bacteremia based on MLST, SCCmec, spa and agr locus types analysis. Microbial Pathogenesis, 2017, 104(3): 328-335. http://doi.org/10.1016/j.micpath.2017.01.055
Hennekinne J., DeBuyser M., Dragacci S. Staphylococcus aureus and its food poisoning toxins: characterization and outbreak investigation. FEMS Microbiology Reviews, 2012, 36(4): 815-836. http://doi.org/10.1111/j.1574-6976.2011.00311.x
Ivanova T., Gurova-Mehmedova E., Daskalov H. Case study of staphylococcal enterotoxin poisoning after consumption of ready-to-eat roasted chicken products. Bulgarian Journal of Agricultural Science, 2017, 23(1): 159-164. Available at: https://www.agrojournal.org/23/01-23.pdf
Jackson C.R., Davis J.A., Barrett J.B. Prevalence and characterization of methicillin-resistant Staphylococcus aureus isolates from retail meat and humans in Georgia. Journal of Clinical Microbiology, 2013, 51(4): 1199–1207. http://doi.org/10.1128/JCM.03166-12.
Kalupahana R.S., Duim B., Verstappen K.M., Gamage C.D., Dissanayake N., Ranatunga L., Graveland H., Wagenaar J.A. MRSA in pigs and the environment as a risk for employees in pig-dense areas of Sri Lanka. Frontiers in Sustainable Food Systems, 2019, 3(2019): 25. http://doi.org/10.3389/fsufs.2019.00025
Kim Y., Kim H., Kim S., Kim M., Kwak H. Prevalence and characteristics of antimicrobial-resistant Staphylococcus aureus and methicillin-resistance Staphylococcus aureus from retail meat in Korea. Food Science of Animal Resources, 2020, 40(5): 758-771. https://doi.org/10.5851/kosfa.2020.e50
Lakhundi S., Zhang K. Methicillin-resistant Staphylococcus aureus: molecular characterization, evolution and epidemiology. Clinical Microbiology Reviews, 2018, 31(4): e00020-18. https://doi.org/10.1128/CMR.00020-18
Lowy F.D. Medical progress: Staphylococcus aureus infections. New England Journal of Medicine, 1998, 339(8): 520-532. https://doi.org/10.1056/NEJM199808203390806
Mahros M., Mohamed S., Khalid A.E., Sallam I. Multidrug-, methicillin-, and vancomycin-resistant Staphylococcus aureus isolated from ready-to-eat meat sandwiches: An ongoing food and public health concern. International Journal of Food Microbiology, 2021, 346(5): 109165. https://doi.org/10.1016/j.ijfoodmicro.2021.109165
Neyra R.C., Frisancho J.A., Rinsky J.L., Resnick C., Carroll K.C., Rule A.M., Ross T., You Y., Price L.B., Silbergeld E.K. Multidrug-resistant and methicillin-resistant Staphylococcus aureus (MRSA) in hog slaughter and processing plant workers and their community in North Carolina (USA). Environmental Health Perspectives, 2014, 122(5): 471-477. http://www.doi.org/10.1289/ehp.1306741
O’Brien A., Hanson B., Farina S., Wu J., Simmering J., Wardyn S., Forshey B., Kulick M., Wallinga D., Smith T. MRSA in conventional and alternative retail pork products. PLoS ONE, 2012, 7(1): e30092. https://doi.org/10.1371/journal.pone.0030092
Özdemir H., Keyvan E. Isolation and characterisation of Staphylococcus aureus strains isolated from beef, sheep and chicken meat. Ankara Üniversitesi Veteriner Fakültesi Dergisi, 2016, 63(4): 333-338. https://doi.org/10.1501/Vetfak_0000002749
Pu S., Han F., Ge B. Isolation and characterization of methicillin-resistant Staphylococcus aureus from Louisiana retail meats. Applied and Environmental Microbiology, 2009, 75(1): 265-267. http://doi.org/10.1128/AEM.01110-08
Sadi A., Samad M., Saddam, Basharat N., Ali S., Roohullah, Saad Z., Khan A.N., Ahmad Y., Khan A. and Khan J. Methicillin-resistant Staphylococcus aureus (MRSA) in slaughter houses and meat shops in capital territory of Pakistan during 2018–2019. Frontiers in Microbiology, 2020, 11(9): 577707. http://doi.org/10.3389/fmicb.2020.577707
Studenica A., Märtlbauer E., Mulliqi-Osmani G. The prevalenceof bacterial contaminants in artisanal cheese sold in informal markets. The case of Kosovo. Food Science and Applied Biotechnology, 2022, 5(1): 77-86. https://doi.org/10.30721/fsab2022.v5.i1.168
Tacconelli E. Methicillin-resistant Staphylococcus aureus: Source control and surveillance organisation. Clin Microbiol Infect, 2009, 15: 31-38. https://doi.org/10.1111/j.14690691.2009.03096.x
Tang Y., Larsen J., Kjeldgaard J., Andersena S.P., Skov R., Ingmera H. Methicillin-resistant and –susceptible Staphylococcus aureus from retail meat in Denmark. International Journal of Food Microbiology, 2017, 246(5): 72-76. https://doi.org/10.1016/j.ijfoodmicro.2017.03.001
Tanomsridachchai W., Changkaew K., Changkwanyeun R., Prapasawat W., Intarapuk A., Fukushima Y., Yamasamit N., Flav Kapalamula T., Nakajima C., Suthienkul O., Suzuki Y. Antimicrobial resistance and molecular characterization of methicillin-resistant Staphylococcus aureus isolated from slaughtered pigs and pork in the Central region of Thailand. Antibiotics, 2021, 10(2): 206. https://doi.org/10.3390/antibiotics10020206
Tiemersa E.W., Bronzwaer SLAM, Lyytikainen O., Degener J.E., Schrijnemakers P., Bruinsma N., Monen J., Witte W., Grundmann H. European antimicrobial resistance surveillance system participants. Methicillin-resistance Staphyloccus aureus in Europe, 1999-2002. Emerging Infectious Diseases, 2004, 10(9): 1627-1634. http://doi.org/10.3201/eid1009.040069
van Duijkeren E., Ikawaty R., Broekhuizen Stins M.J., Jansen M.D., Spalburg E.C., deNeeling A.J., Allaart J.C., van Nes A., Wagenaar J.A., Fluit A.C. Transmission of methicillin-resistant Staphylococcus aureus strains between different kinds of pig farms. Veterinary Microbiology, 2008, 126(4): 383-389. https://doi.org/10.1016/j.vetmic.2007.07.021
van Loo H.M., Diederen M.W., Savelkoul P., Woudenberg J., Roosendaal R., van Belkum A., Lemmens-den Toom N., Verhulst C., van Keulen P., Kluytmans J. Methicillin-Resistant Staphylococcus aureus in meat products, the Netherlands. Emerging Infectious Diseases, 2007, 13(11): 1753-1755. http://doi.org/10.3201/eid1311.070358 Weese J.S., Avery B.P., Reid-Smith R.J. Detection and quantification of methicillin-resistant Staphylococcus aureus (MRSA) clones in retail meat products. Letters in Applied Microbiology, 2010, 51(3): 338-342. https://doi.org/10.1111/j.1472-765X.2010.02901.x
Wells M., Juett B. Prevalence of MRSA on meat products in central Kentucky. Bios, 2012, 83(1): 33-38. https://www.jstor.org/stable/23267857
Wu S., Huang J., Wu Q., Zhang J., Zhang F., Yang X., Wu H., Zeng H., Chen M., Ding Y et al. Staphylococcus aureus isolated from retail meat and meat products in China: Incidence, antibiotic resistance and genetic diversity. Frontiers in Microbiology, 2018, 9(11): 02767. http://doi.org/10.3389/fmicb.2018.02767
Wu S., Huang J., Zhang F., Wu Q., Zhang J., Pang R., Zeng H., Yang X., Chen M., Wang J., Dai J., Xue L., Lei T., Wei X. Prevalence and characterization of food-related methicillin-resistance Staphylococcus aureus (MRSA) in China. Frontiers in Microbiology, 2019, 10(2): 00304. https://doi.org/10.3389/fmicb.2019.00304
Wu S, Zhang F, Huang J, Wu Q, Zhang J, Dai J, Zeng H, Yang X, Chen M, Pang R et al. Phenotypic and genotypic characterization of PVL-positive Staphylococcus aureus isolated from retail foods in China. International Journal of Food Microbiology, 2018, 304(9): 119-126. http://doi.org/10.1016/j.ijfoodmicro.2019.05.021
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How to Cite
KRUMOVA-VALCHEVA, Gergana Lyubomirova.
The role of food in the spread of the Methicillin – resistant Staphylococcus aureus (MRSA).
Food Science and Applied Biotechnology, [S.l.], v. 6, n. 1, p. 87-94, mar. 2023.
ISSN 2603-3380.
Available at: <https://www.ijfsab.com/index.php/fsab/article/view/238>. Date accessed: 12 sep. 2024.
doi: https://doi.org/10.30721/fsab2023.v6.i1.238.